Neotropical Ichthyology, 10(3):653-659, 2012 Copyright © 2012 Sociedade Brasileira de Ictiologia

Parasitism by argulids (Crustacea: ) in piranhas (Osteichthyes: Serrasalmidae) captured in the Caiçara bays, upper Paraguay River, Pantanal, Mato Grosso State, Brazil

Márcio Fontana1, Ricardo Massato Takemoto2, José Celso de Oliveira Malta3 and Lúcia Aparecida de Fátima Mateus4

In this study, 446 fishes were analyzed: 190 Pygocentrus nattereri, 193 Serrasalmus maculatus, and 63 S. marginatus.They were captured in two bays, upper and lower Caiçara, in the upper Paraguay River basin, during one hydrological cycle from May 2008 to April 2009. Six species of Branchiura were found: Dolops bidentata, D. longicauda, Dolops sp., Argulus multicolor, A. chicomendesi, and Dipteropeltis hirundo. All fish species were infested by more than one species of Branchiura and the overall prevalence was 33.4%. The following prevalences were observed: 52.6% in P. nattereri; 20.3% in S. maculatus, and 15.8% in S. marginatus. The relative condition factor (Kn) differed significantly between parasitized and non parasitized individuals only in P. nattereri and S. maculatus. There was no correlation between Kn and abundance of parasites nor between body length (Ls) and intensity of infestation, in all three host species.

Foram analisados 446 peixes: 190 Pygocentrus nattereri, 193 Serrasalmus maculatus e 63 S. marginatus, capturados nas baías Caiçara superior e inferior na bacia do alto rio Paraguai, durante um ciclo hidrológico nos meses de maio de 2008 a abril de 2009. Foram encontradas seis espécies de Branchiura: Dolops bidentata, D. longicauda, Dolops sp., Argulus multicolor, A. chicomendesi e Dipteropeltis hirundo. Todos os peixes estavam parasitados por mais de uma espécie de Branchiura e a prevalência geral foi 33,4%. As prevalências foram: P. nattereri 52,6%, S. maculatus 20,3% e S. marginatus 15,8%. O fator de condição relativo (Kn) diferiu significativamente entre indivíduos parasitados e não parasitados apenas em P. nattereri e S. maculatus. Não houve correlação significativa entre Kn e abundância de parasitos, nem entre comprimento padrão (Ls) e intensidade de infestação, nas três espécies de piranhas analisadas.

Key words: Argulus, Dolops, Pygocentrus, Relative condition factor, Serrasalmus.

Introduction rate (Crowden & Broom, 1980; Milinski, 1984), greater vulnerability to predators (Arme & Owen, 1967) and decreased resistance to One of the main challenges of ecology is to clarify the role of environmental stress (Lewis & Hettler, 1968). The relative parasites in the host’s population dynamics (Begon et al., 2007). condition factor (Kn) is a quantitative indicator of fish well-being, The relationship between fish and parasites in the natural therefore the analysis of its variability between populations and environment is an important tool for the understanding of individuals can show the effects of parasitisation (Ranzani-Paiva pathologies occurring in hosts, and are also relevant to et al., 2000). Many studies on the biology of endoparasites have pisciculture (Tavares-Dias et al., 2000). Aquatic environments been conducted in Osteichthyes. However, little information is facilitate reproduction, dispersion and survival of parasitic available on the infestation levels and modes of transmission of organisms (Malta, 1984). Direct effects, such as host impairment, ectoparasites in natural conditions (Szalai & Dick, can induce indirect consequences such as reduction in foraging 1991). Most studies on branchiuran crustacean ectoparasites

1Universidade Federal de Mato Grosso, Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade, Instituto de Biociências. Av. Fernando Correa da Costa, s/n°, Bairro Boa Esperança, 78060-900 Cuiabá, MT, Brazil. [email protected] 2Universidade Estadual de Maringá, Núcleo de Pesquisas em Limno1ogia, Ictiologia e Aquicultura, Laboratório de Ictioparasitologia. Av. Colombo, 5790, Bloco G-90, sala 11, 87020-900 Maringá, PR, Brazil. [email protected] 3Instituto Nacional de Pesquisas da Amazônia - INPA, Laboratório de Parasitologia de Peixes, Cx. Postal 478, 69011-970 Manaus, Amazonas, Brazil. [email protected] 4Universidade Federal de Mato Grosso, Laboratório de Ecologia e Manejo de Recursos Pesqueiros, Instituto de Biociências. Av. Fernando Correa da Costa, s/n°, Bairro Boa Esperança, 78060-900 Cuiabá, MT, Brazil. [email protected]

653 654 Parasitism by argulids (Crustacea: Branchiura) in piranhas published in South America are related to taxonomy (Malta, 1982a; and lower Caiçara Bay (LCB), located on the south east bank Tanaka, 2000). The Branchiura is a small group of ectoparasites, of the Paraguay River, between coordinates 16°05’02.8”S comprising a single family (), with only four genera, 57°44’22.7”W and 16°06’41.9”S 57°45’14.6”W (Fig. 1). i.e., Argulus, Dolops, Dipteropeltis, and Chonopeltis. Are commonly known as fish lice and are characterized by their dorso- Sampling and data analysis ventrally flattened bodies, which are covered by a horseshoe- Monthly collections were performed during a hydrological shaped dorsal cephalic shield formed by the carapace lobes. Its cycle from May 2008 to April 2009. Collections were made only posterolateral lobes extend over the four pairs of thoracic during the day and the piranhas were captured in six different biramous legs to a greater or lesser extend depending on the points (UCB: P1, P2, P3; LCB: P4, P5, P6) and in two species. Five pairs of cephalic appendages occur ventrally, i.e., microhabitats: margin and middle, of both bays (Fig.1). Weight, antennulae (absent or reduced in Chonopeltis), antennae, standard length and gender of the hosts were recorded. mandibles, maxillulae, and maxillae. The antennulae bear a small Necropsy of the hosts, collection, conservation and preparation hook terminally. There are approximately 210 species (Moller et of ectoparasites were performed according to the method of al., 2007). They are all parasites of fishes but on rare occasion Malta (1982a). The standard length (Ls) and total weight (Wt) have been reported from alligators (Ringuelet, 1943), tadpoles of each host were adjusted to the Wt/Ls relationship curve (Stuhlmann, 1891; Wolfe et al., 2001), and salamanders (Poly, (Wt = a.Ltb), given the estimated values of the regression 2003). Dipteropeltis was described in 1912 (Calman, 1912) and coefficients a and b. The variables a and b were used to estimate since its description, a limited number of reports appeared the expected weight (We), using the equation: We = a.Ltb. The sporadically. Information on this genus is therefore very limited. relative condition factor (Kn) was calculated, according to the The adults range between 5 and 15 mm in size although quotient between observed weight and expected weight for a Dipteropeltis may reach up to 30 mm (Piasecki & Oldewage, given length (Kn = Wt / We) (Le Cren, 1951). The Mann- 1992).The transmission is direct and the parasites actively swim Whitney test (U) was used to determine differences in Kn to find a host in which they will be fixed to its body surface between parasitized and non-parasitized (Zar, 1996). To eliminate (Malta & Varella, 1983).The fish ectoparasites Branchiura the interference of gonadal weight on the Kn, the infected and (Crustacea) display two different ways of attachment to the fish uninfected hosts were divided into two groups: mature- surface as adults: the first maxillae are either hooks (Dolops) or maturation and rest-depleted-immature.Spearman’s rank suction discs (Argulus, Chonopeltis, and Dipteropeltis) (Moller correlation coefficient (rs) was used to assess possible et al., 2008). According to Piasecki & Oldewage (1992), the correlations between Kn and intensity of infestation, as well as maxillulae are transformed into powerful suckers in the adults intensity of infestation and host length (Zar, 1996). The Kruskal- and are utilized to attach to their hosts except in Dolops, where Wallis test (H) was applied to compare mean intensity values the maxillulae bear strong hooks that penetrate the host for of branchiuran species between hosts. In order to compare the attachment. In general, the infestation results in ulcerous lesions that allow secondary infections by fungi, viruses, and bacteria (Thatcher, 2006). Species of Serrasalmidae are among the main predators that thrive in Neotropical freshwater ecosystems (Almeida et al., 1998). Piranhas represent a large percentage of the number of individuals and the total biomass of Osteichthyes where they live (Mago-Leccia, 1970). Because of that, many studies have been conducted on the interaction between piranhas and their crustacean ectoparasites (Malta, 1982b; Malta & Varella, 1983; Carvalho et al., 2003). The aim of this study is to assess parasitism by argulids in Pygocentrus nattereri Kner, 1858, Serrasalmus maculatus Kner, 1858 and Serrasalmus marginatus Valenciennes, 1837, in two bays, upper and lower Caiçara, in the upper Paraguay river basin, in Pantanal, Mato Grosso State, Brazil, during one hydrological cycle from May 2008 to April 2009.

Material and Methods

Study site Located in western Brazil, the Pantanal is the largest continuous freshwater floodplain in the world (Silva & Abdon, Fig. 1. Location of collection sites in the upper Caiçara bay 1998). Collections were made in the upper Paraguay River (UCB - Points 1, 2 and 3) and lower Caiçara bay (LCB - Points basin, Northern Pantanal, Cáceres municipality, Mato Grosso 4, 5 and 6), upper Paraguay River basin, Pantanal, Mato State, Brazil. Two bays were sampled: upper Caiçara Bay (UCB) Grosso, Brazil. M. Fontana, R. M. Takemoto, J. C. O. Malta & L. A. F. Mateus 655 frequency of branchiuran species according to attachment sites Branchiura species parasitizing P. nattereri, S. maculatus, and on hosts, the Independence Test of Chi-square (χ2) was used S. marginatus (male and female) are shown in Table 3. on the data in a contingency table. The statistical significance In the dry climatic station, the average rate of oxygen level adopted was 0.05. The prevalence, mean intensity, dissolved in water was 6.4 mg / l (range: 4.64 - 7.84 mg / l) and abundance and amplitude of infestation concepts were used the rainy season the average was 3.5 mg / l (range: 0.94 - 5.62 according to Bush et al. (1997). Voucher specimens of hosts mg/l).There was a significant difference between Kn of were deposited in the Fish Collection at the Departamento de parasitized and non-parasitized P. nattereri (Z[U] = 1.72; p = Biologia e Zoologia of the Universidade Federal do Mato Grosso 0.042) and S. maculatus (Z[U] = 8.08 ; p = 0.001). There was (Serrasalmus maculatus, CPUFMT 686; Pygocentrus nattereri, no significant difference in S. marginatus (Z[U] = 0.02 ; p = CPUFMT 687 / CPUFMT 688; and Serrasalmus marginatus, 0.492) (Fig. 2). CPUFMT 689). The Branchiura voucher specimens are in the In addition, there was no strong relationship between Kn Collection of non- Invertebrates of the Instituto Nacional and infestation intensity by Branchiura in all three piranha de Pesquisas da Amazônia (Dipteropeltis hirundo, INPA 1873; species (P. nattereri: rs = 0.152; p = 0.129, S. maculatus: rs = Dolops longicauda, INPA1956; Dolops bidentata, INPA1957; 0.19; p = 0.231 and S. marginatus: rs = 0.52; p = 0.121). The Dolops sp., INPA1958; Argulus multicolor, INPA1959 / correlation between the length of hosts and infestation INPA1960 / INPA1962; and Argulus chicomendesi, INPA1961). intensity by Branchiura was not significant (P. nattereri: rs = - 0.0313 and p = 0.62; S. maculatus: rs = - 0.060 and p = 0.64; S. Results marginatus: rs = 0.286 and p = 0.21) (Fig. 3). The Kruskal-Wallis test (H) did not show significant In total, 190 individuals of Pygocentrus nattereri were differences in the mean intensity values between Branchiura captured (male = 128; female = 62), 193 of Serrasalmus maculatus species and host species (H = 6.6; p = 0.085). However, the (male = 84; female = 109) and 63 of S. marginatus (male = 37; frequency of species of Branchiura attached in different sites female = 26). Six Branchiura species were recorded: Dolops of hosts showed considerable variation (χ2 = 27.62; p = 0.0062). bidentata (Bouvier, 1899), D. longicauda (Heller, 1857), Dolops The highest infestation rate was recorded in the peri-opercular sp., Dipteropeltis hirundo Calman, 1912, Argulus multicolor region, pectoral and pelvic fins. Stekhoven, 1937 and A. chicomendesi Malta & Varella, 2000. Dolops longicauda and D. hirundo occurred only once on S. Discussion maculatus. Dolops bidentata showed the highest prevalence in P. nattereri (male and female) during drought (April-September) Branchiura are fish ectoparasites. They attach themselves and the rainy season (October-March), in two bays. A. multicolor to the body surface, fin base, branchial and mouth cavities of and A. chicomendesi had the lowest prevalence during the dry their hosts (Castro, 1950; Yamaguti, 1963; Malta, 1982a, b). period and did not occur during the rainy season, in two bays. Attachment to the host is facilitated by suckers or hooks on The prevalence rates of infestation are shown in Table1. the maxillulae as well as the hooks on the antennulae (Piasecki During the study period, in dry season, there was a greater & Oldewage, 1992).In this study, six Branchiura species: mean intensity infestation and abundance by Dolops bidentata Dolops bidentata, D. longicauda, Dolops sp., Argulus on Pygocentrus nattereri (male and female). The lowest values multicolor, A. chicomendesi, and D. hirundo, were recorded were recorded by Argulus multicolor and A. chicomendesi on for the first time parasitizing three species of piranhas, three host species. No specimen from A. multicolor was found Pygocentrus nattereri, Serrasalmus maculatus and S. parasitizing S. maculatus (male and female), in this climatic marginatus captured in the upper Paraguay river. Dolops station. (Table 2.). In the rainy season there was no record of longicauda was not considered for statistical purposes any specimen of A. multicolor and A. chicomendesi in males because there was only one specimen (female, whose body and females for the three host species. During the rainy season was full of eggs).The first record of D. longicauda in the one specimen of D. bidentata and one Dolops sp. parasitizing Paraguay River was near Cáceres (Moreira, 1913). Dolops S. marginatus were found. Parasitological rates of the bidentata was first reported in the Cuiabá River (Silva-Souza

Table 1. Prevalence (%) of Branchiura species parasitizing Pygocentrus nattereri, Serrasalmus maculatus, and Serrasalmus marginatu captured in the Caiçara bays, upper Paraguay River basin, Pantanal, Mato Grosso, Brazil, from May 2008 to April 2009. Prevalence (%) Weather station Parasite/ Host P. nattereri S. maculatus S. marginatus male female male female male female Dry D. bidentata 56.5 35.7 26.5 23.3 18.2 0.0 (April-September) Dolops sp. 27.1 10.7 16.3 6.7 9.1 25.0 A. multicolor 1.2 7.1 0.0 3.3 4.5 0.0 A. chicomendesi 1.2 0.0 0.0 0.0 4.5 0.0 Rainfall D. bidentata 20.9 50.0 2.9 7.6 0.0 9.1 (October-March) Dolops sp 11.6 11.8 5.7 5.1 0.0 4.5 656 Parasitism by argulids (Crustacea: Branchiura) in piranhas

Table 2. Parasitological rates of the Branchiura species parasitizing Pygocentrus nattereri, Serrasalmus maculatus, and Serrasalmus marginatus captured in the Caiçara bays, upper Paraguay River basin, Pantanal, Mato Grosso, Brazil, during dry season (April to September 2008). MI = mean intensity; SD = Standard deviation; Amp = amplitude; MA = mean abundance.

Weather station Dry male female Host/ Parasites MI ± SD MA ± SD Amp MI ± SD MA ± SD Amp P. nattereri D. bidentata 3.6±3.3 2.10±2.8 1-22 1.7±0.7 0.60±0.6 1-3 Dolops sp. 1.4±0.5 1.00±0.3 1-3 1.0±0.0 0.10±0.0 1 A. multicolor 3.0±0.0 0.04±0.0 1-3 - - - A. chicomendesi 1.0±0.0 0.01±0.0 1 1.0±0.0 0.10±0.0 1 S. maculatus D. bidentata 2.8±1.6 0.80±1.1 1-6 2.3±1.3 0.50±0.8 1-5 Dolops sp. 1.3±0.3 0.20±0.2 1-2 2.0±1.4 0.10±0.5 1-3 A. chicomendesi - - - 1.0±0.0 0.03±0.0 1 S. marginatus D. bidentata 1.8±0.5 0.30±0.3 1-2 - - - Dolops sp. 1.0±0.0 0.10±0.2 1 1.0±0.0 0.30±0.0 1 A. multicolor 1.0±0.0 0.05±0.0 1 - - - A. chicomendesi 1.0±0.0 0.05±0.0 1 - - -

et al., 2011). Dolops hirundo was first recorded in the Miranda station. One factor likely to affect the dynamics of infestation and Abobral rivers, Pantanal of Mato Grosso do Sul (Carvalho for Branchiura in hosts may be the reproductive hormonal et al., 2003) and was found in the Lower Caiçara Bay in only influence. Thomas (1964) and Pennycuick (1971) suggested one sample (female, without eggs in the thorax), being that the low incidence of parasites during the spawning fish, insufficient in number for further exploration of the species. which coincided with the period of rainfall, may be due to the Argulus multicolor was recorded in the Kuluene and Xingu presence of estrogen, a hormone that appears in the blood of rivers in Mato Grosso state (Castro, 1949). Argulus the fish during maturation. After spawning, this hormone chicomendesi was first collected in Janauacá Lake, on the decreases, and the opposite effect happens. In the same southeast bank of the Solimões River bank in Amazonas state context, William (1965) noted that Calicotyle kroyeri (Malta & Varella, 2000). Also in this study, it was recorded for (Trematoda: Monogenea) was never present in pregnant Raja the first time A. chicomendesi parasitizing fish in Mato Grosso radiata (Rajiformes: Rajidae), while the non-pregnant females state.The infestation showed a seasonal pattern with a high showed this parasite. Is it speculated that with the decrease prevalence of D. bidentata and Dolops sp. in the dry season of water in the bays concentrated the host and therefore (April-September) on P. nattereri and S. maculatus. This increased habitat availability (host body) for attaching occurred when ideal conditions prevailed with high dissolved Branchiura. Poor health, decreased reproductive efficiency oxygen concentrations in the water and when hosts species were more abundant. There was no synchronization between the reproductive period of hosts. Reproduction of piranhas occurred during the rainy station and Branchiura in the dry

Table 3. Parasitological rates of the Branchiura species parasitizing Pygocentrus nattereri, Serrasalmus maculatus and Serrasalmus marginatus captured in the Caiçara bays, upper Paraguay River basin, Pantanal, Mato Grosso, Brazil, during rainfall season (October 2008 to March 2009). MI=mean intensity; SD=Standard deviation; Amp=amplitude; MA=mean abundance.

Weather station Rainfall Host/ male female Parasites MI ± SD MA ± SD Amp MI ± SD MA ± SD Amp P. nattereri Fig. 2. Box-plot of Kn values in parasitized and non-parasitized D. bidentata 1.7±0.8 0.30±0.5 1-4 2.1±0.9 1.00±0.7 1-4 individuals of Pygocentrus nattereri, Serrasalmus maculatus Dolops sp. 1.2±0.3 0.10±0.1 1-2 1.0±0.0 1.00±0.0 1 S. maculatus and Serrasalmus marginatus captured in the upper and lower D. bidentata 1.0±0.0 0.03±0.0 1 2.3±1.2 0.20±0.5 1-4 Caiçara bays, upper Paraguay River basin, Pantanal, Mato Dolops sp. 1.0±0.6 0.10±0.2 1-2 1.8±0.6 0.10±0.2 1-3 Grosso, Brazil. M. Fontana, R. M. Takemoto, J. C. O. Malta & L. A. F. Mateus 657

Fig. 3. Correlation between Standard length (Ls) and intensity (Int.) of infestation in Pygocentrus nattereri, Serrasalmus maculatus, and Serrasalmus marginatus captured in the upper and lower Caiçara bays, upper Paraguay River basin, Pantanal, Mato Grosso, Brazil. and feeding conversion are among the negative effects on explain the highest incidences of branchiuran species in P. hosts (Bauer, 1961). However, the effects that pathogenic nattereri and S. maculatus. Serrasalmus marginatus is a agents have on fish are difficult to assess or quantify, territorial species and patrols feeding sites in areas of 3 to 4 especially in natural conditions (Chubb, 1973). According to m2 (Sazima & Machado, 1990). They show lower prevalence, Le Cren (1951), the condition factor is a quantitative indicator possibly due to the fact that they do not show gregarious of fish fitness, reflecting recent feeding conditions and is behavior and are territorials. In addition, some ectoparasite obtained using the weight-length relation of the individual. species are found in greater quantities on larger fish. This According to Brasil-Sato & Pavanelli (1999) and Lizama et al. indicates that the parasite burden can vary in proportion (2006), the relative condition factor can be used as a tool for related to the age and size of the hosts, given the longer studies of the relationship between the host’s health and exposure period and larger surface area for parasitic level of parasitism. In this study Pygocentrus nattereri and aggregation (Cloutman & Becker, 1977; Hanek & Fernando, Serrasalmus maculatus show significant differences in 1978; Poulin, 1991). In P. nattereri, S. spilopleura (= condition factor between parasitized and non-parasitized fish. Serrasalmus maculatus in Paraguay River) and S. marginatus However, S. marginatus (parasited or not) showed better body captured in Miranda River, Pantanal of Mato Grosso do Sul, condition compared to P. nattereri and S. maculatus, the correlation between body length and the incidence of suggesting better adaptation to the actions of Branchiura ectoparasites was not significant (Carvalho et al., 2003). species. Normally endoparasites reach their hosts through Avenant & Van As (1985) reported that the occurrence of feeding, while ectoparasites find a host through their ability Dolops ranarun is linked to the distribution of the two major to swim during their juvenile stages or through their close hosts, Oreochromis mossambicus (Perciformes: Cichlidae) and proximity to their hosts (Begon et al., 2007). For many Clarias gariepinus (Siluriformes: Clariidae). In this study, the organisms, life in groups can be an advantage, reducing correlation between size of the fish and intensity of infestation predation risk and improving foraging capacity (Wilson, 2000). was not significant in fish from the UCB and LCB. Parasitic However, there is greater risk of exposure to parasites given species generally select special microhabitats or tissues to the close proximity of individuals (Alcock, 2001).This is attach to, suggesting a wide opportunity of differentiation of especially true for fishes that swim in schools (Poulin, 1991). niches (Begon et al., 2007). The transmission of argulids is In the Cuiabá River, in the Pantanal of Mato Grosso, a study direct since they actively swim to find a host to attach to. was carried out using underwater observations. The authors They can leave the host at any time and move to another fish. registered P. nattereri swimming in schools of 20 to 30 They can also slide over the surface of the fish in order to individuals and S. spilopleura (= Serrasalmus maculatus in find an appropriate site for feeding (Thatcher, 2006). The Paraguay River) in schools of up to 20 fish (Sazima & largest number of branchiuran individuals was found in the Machado, 1990). Pygocentrus nattereri and S. spilopleura ventral body area of P. nattereri (Sazima & Machado, 1990). (= Serrasalmus maculatus in Paraguay River) are sympatric In this study, the cranio-ventral area (gullet region which species (Behr & Signor, 2008). The gregarious or solitary incorporates pectoral and pelvic fins) and the peri-opercular behaviors were the main factors determining the structure of area were the sites where most Branchiura occurred in the the parasites infra-communities in S. spilopleura (= three host species. Barnard (1955) reported the presence of Serrasalmus maculatus in Paraguay River), a gregarious Dolops ranarum in the mouth cavity and gill chamber of O. species, and S. marginatus, a non-gregarious species (Tanaka, mossambicus. Analysis of attachment site preference of 2000). Gregarious habits, size of schools and sympatry are crustacean ectoparasites was carried out by Bulow et al. (1979) facilitating factors in parasitic transmission of ectoparasites for the Lernaea cyprinacea Linnaeus on stream fish. in fish with gregarious behavior. These factors may help to These authors divided the body into different regions and 658 Parasitism by argulids (Crustacea: Branchiura) in piranhas found that L. cyprinacea preferred sheltered areas for Bulow, F. J., Winningham, J. R. & Hooper, R. C. 1979. Occurrence attachment. Kruger et al. (1983) investigated site selection of of the copepod parasite Lernaea cyprinacea in a stream fish the branchiuran and also divided the body population.Transactions of the American Fisheries Society, 108: into different regions. These authors did not find any distinct 100-102. pattern as to site selection on the body of host fish. Avenant Bush, A. O., K. D. Lafferty, J. M. Lotz & A. W. Shostak. 1997. Parasitology meets ecology on its own terms. Journal of & Van As (1985) evaluated the preference of attachment site Parasitology, 84: 575-583. of D. ranarum from information collected at various localities Carvalho, L. N., K. Del-Claro & R. M.Takemoto. 2003. Host-parasite during winter, spring and summer and no significant pattern interaction between branchiurans (Crustacea: Argulidae) and pi- related to location or season could be observed concerning ranhas (Osteichthyes: Serrasalminae) in the Pantanal wetland of site selection on any of different host fish. According to Fryer Brazil. Environmental Biology of Fishes, 67: 289-296. (1968), D. ranarum shows a distinct preference for the buccal Calman, W. T. 1912. On Dipteropeltis a new genus of the crustacean cavity and its extensions on scaled fish, but is also found on Order Branchiura. Proceedings of the Zoological Society of the skin of smooth-skinned fish. This study demonstrates London, 4: 763-766. that behavior of the hosts can influence, directly or indirectly, Castro, A. L. 1949. Contribuição ao conhecimento dos crustáceos argulídeos do Brasil (Branchiura: Argulidae) com descrição de the structure of Branchiura community. However, it is still uma nova espécie. Boletim do Museu Nacional. Nova Série: important to assess if reproductive factors, as well as Zoologia, 93: 1-8. environmental factors controlling changes in flooding basin Castro, A. L. 1950. Contribuição ao conhecimento dos argulídeos do of the Paraguay River, also influence host-parasite Brasil. Descrição de duas novas espécies. Academia Brasileira de relationships. Ciências, 22: 245-255. Chubb, J. C. 1973. Influence of parasites on freshwater fishes in Acknowledgements Britain. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie, 18: 1628-1632. Cloutman, D. G. & D. A. Becker. 1977. Some ecological aspects of The authors would like to thank Jansen Zuanon (INPA) Ergasilus centrarchidarum Wright (Crustacea: Copepoda) on for the taxonomic identification of host fishes. largemouth and spotted bass in Lake Fort Smith. Journal Parasitology, 63: 372-376. Literature Cited Crowden, A. E. & D. M. Broom. 1980. Effects of the eyefluke, Diplostomum spathaceum, on the behaviour of dace (Leuciscus Alcock, J. 2001. Behavior: An Evolutionary Approach. leuciscus). Animal Behaviour, 28: 287-294. Maryland, Sinauer Associates, 543p. Fryer, G. 1968. The parasitic Crustacea of African freshwater fishes; Almeida, V. L. L., N. S. Hahn & C. S. Agostinho. 1998. Stomach their biology and distribution. Journal of Zoology London, 156: content of juvenile and adult piranhas (Serrasalmus marginatus) 45-95. in the Paraná Floodplains, Brazil. Studies on Neotropical Fauna Hanek, G. & C. H. Fernando. 1978. The role of season, habitat, host and Environment, 33: 100-105. age and sex on gill parasites of Lepomis gibbosus (L). Canadian Arme, C. & R. W. Owen, 1967. Infections of the three-spined Journal Zoology, 56: 1247-1250. , Gasterosteous aculeatus L. with the plerocercoid Kruger, I., Van As, J. G. & Saayman, J. E. 1983. Observations on the larvae of Schistocephalus solidus (Muller, 1776), with special occurrence of the fish lice Argulus japonicus Thiele, 1990 in the reference to pathological effects. Parasitology, 57: 301-314. western Transvaal. South African Journal of Zoology, 18: 408-410. Avenant, A. & J. G. Van As. 1985.Occurrence and distribution of Le Cren, E. D. 1951. The length-weight relationship and seasonal Dolops ranarum Stuhlmann, ectoparasite of freshwater fish in cycle in gonad weight and condition in the perch Perca fluviatilis. the Transvaal, South Africa. Journal Fish Biology, 27: 403-416. Journal of Animal Ecology, 20: 201-219. Barnard, K. H. 1955. South African parasitic Copepoda. Annals of Lewis, R. M. & W. F. Hettler. 1968. Effects of temperature and the South African Museum, 41: 223-312. salinity on the survival of young Atrantic menhaden, Brevoortia Bauer, O. N. 1961. Relationships between host fishes and their tyrannus. American Fisheries Society, 97: 344-349. parasites. Pp. 84-103. In: Dogiel ,V. A., G. K. Petrushevski & Y. Lizama, M. de Los A. P., R. M. Takemoto & G. C. Pavanelli. 2006. I. Polyanski (Eds.). Parasitology of fishes. Edinburgh, Leningrad Parasitism influence on the hepato, splenosomatic and weight/ University Press, 384p. lenght relation and relative condition factor of Prochilodus Begon, M., C. R. Townsend & J. L. Harper. 2007. Parasitismo e lineatus (Valenciennes, 1836) (Prochilodontidae) of the upper doença. Pp. 347-380. In: Begon, M., C. R. Townsend & J. L. Paraná river floodplain, Brazil. Revista Brasileira de Parasitologia Harper (Eds.). Ecologia de Indivíduos a Ecossistemas. Porto Veterinária, 15: 116-122. Alegre, Artmed, 740p. Mago-Leccia, F. 1970. Estudios preliminares sobre la ecología de Behr, E. R. & C. A. Signor. 2008. Distribuição e alimentação de duas los peces de los llanos. Acta Biológica, 7: 71-102. espécies simpátricas de piranhas Serrasalmus maculatus e Malta, J. C. O. 1982a. Os argulídeos (Crustacea: Branchiura) da Pygocentrus nattereri (Characidae: Serrasalminae) do rio Ibicuí, Amazônia Brasileira. Aspectos da ecologia de Dolops discoidalis Rio Grande do Sul, Brasil. Iheringia, 98: 501-507. Bouvier, 1899 e Dolops bidentata Bouvier, 1899. Acta Brasil-Sato, M. C. & G. C. Pavanelli. 1999. Ecological and Amazonica, 12: 521-528. reproductive aspects of Neoechinorhynchus pimelodi Malta, J. C. O. 1982b. Os argulídeos (Crustacea: Branchiura) da (Eoacantocephala, Neoechinorhynchidae) of Pimelodus Amazônia Brasileira, 2. Aspectos da ecologia de Dolops geagy maculatus Lacépède (Siluroidei, Pimelodidae) of the São Fran- Bouvier, 1897 e Argulus juparanaensis Castro, 1950. Acta cisco River, Brazil. Revista Basileira de Zoologia, 16: 73-82. Amazonica, 12: 701-705. M. Fontana, R. M. Takemoto, J. C. O. Malta & L. A. F. Mateus 659

Malta, J. C. O. 1984. Os Peixes de um lago de várzea da Amazônia Sazima, I. & F. A. Machado. 1990. Underwater observations of Central (Lago Janauacá, Rio Solimões) e suas relações com os piranhas in western Brazil. Environmental Biology of Fishes, crustáceos ectoparasitos (Branchiura: Argulidae). Acta 28: 17-31. Amazonica, 14: 355-372. Silva-Souza, A. T., V. D. Abdallah, R. K. de Azevedo, F. A. da Silva Malta, J. C. O. & A. M. B. Varella. 1983. Os argulídeos (Crustacea: & J. L. Luque. 2011. Expanded Description of Dolops bidentata Branchiura) da Amazônia Brasileira 3. Aspectos da ecologia de (Bouvier, 1899) (Branchiura: Argulidae) based on specimens Dolops striata Bouvier, 1899 e Dolops carvalhoi Castro, 1949. collected on Pygocentrus nattereri Kner, 1858 (Characiformes) Acta Amazonica, 13: 299-306. from Poconé Wetland, MT, Brazil. Brazilian Journal of Biology, Malta, J. C. O. & A. M. B. Varella. 2000. Argulus chicomendesi 71: 145-149. sp. n. (Crustacea: Argulidae) parasita de peixes da Amazônia Silva, J. S. V. & M. M. Abdon. 1998. Delimitação do Pantanal brasileira. Acta Amazonica, 30: 481-498. Brasileiro e suas sub-regiões. Pesquisa Agropecuária Brasileira, Milinski, M. 1984. Parasites determine a predator’s optimal feeding 33: 1703-1711. strategy. Behavioural Ecology and Sociobiology, 15: 35-37. Stuhlmann, F. 1891. Zur kenntniss der Fauna central-afrikanischer Moller, O. S., J. Olesen & D. Waloszek. 2007. Swimming and cleaning Seen II. Ueber eine neue Art der Arguliden-Gattung Gyropeltis. in the free-swimming phase of Argulus larvae (Crustacea: Zoologische Jahrburcher, Abteilung für Systematik, 5: 152-154. Branchiura) - Appendage adaptation and functional morphology. Szalai, A. J. & T. A. Dick. 1991. Evaluation of gill nets, fyke nets, and Journal of Morphology, 268: 1-11. mark-recapture methods to estimative the number of hirudinea Moller, O. S., J. Olsen, A. Avenant-Oldewage, P. F. Thomsen & H. and crustacea on fish. Journal of Parasitology, 77: 914-922. Glenner. 2008. First maxillae suction discs in Branchiura (Crustacea): Tanaka, L. K. 2000. Aspectos ecológicos dos parasitos de Development and evolution in light of the first molecular phylogeny Serrasalmus marginatus Valenciennes, 1847 e Serrasalmus of Branchiura, Pestastomida, and other “”. spilopleura Kner, 1860 (Characiformes, Serrasalmidae) do rio Structure & Development, 37:333-346. Baía, planície de inundação do alto rio Paraná. Unpublished Moreira, C. 1913. Comissão de Linhas Telegraphicas Estratégicas MSc. Dissertation, Universidade Estadual de Maringá, de Matto-Grosso ao Amazonas: História Natural, Zoologia, Maringá, 32p. Crustáceos. Papelaria Macedo, 5: 10-11. Tavares-Dias, M., M. L. Martins & F. L. Moraes. 2000. Condition Pennycuick, L. 1971. Quantitative effects of three species of parasites factor, hepatosomatic and splenosomatic relation of freshwater on a population of Three-spined , Gasterosteus fishes naturally parasitized. Acta Scientiarum Biological aculeatus. London: Journal Zoology, 165: 143-162. Sciences, 22: 533-537. Piasecki, W. & A. Avenant- Oldewage. 1992. Diseases Caused by Thatcher, V. E. 2006. Amazon Fish Parasites. Branchiura. Pp. 391- Crustacea. Pp. 1162-1174. In: Schäperclaus, W. (Ed.). Fish 415. In: Thatcher, V. E. (Ed.). Amazon Fish Parasites. Bulgaria, Diseases (English translation of ‘Fischkrankheiten’, 5th corrected Pensoft Publishers, 508p. and substantially enlarged edition 1986). A. A. Balkema, Thomas, J. D. 1964. A comparasion between the helminth burdens Rotterdam, 164p. of male and female brown trout, Salmo trutta (L.) from a natural Poly, W. J. 2003. Argulus ambystoma, a new species parasitic on population in River Teify, West Wales. Parasitology, the salamander Ambystoma dumerilii from Mexico (Crustacea: EUA:Cambridge University Press, 54: 263-272. Branchiura: Argulidae). Ohio Journal of Science, 103: 52-61. William, H. H. 1965. Observations on the occurrence of Dictyocotyle Poulin, R. 1991. Group-living and the richness of the parasite fauna coelica and Calicotyle kroyeri (Trematoda: Monogenea). in Canadian freswater fishes. Oecologia, 3: 390-394. Parasitology, EUA: Cambridge University Press, 55:201-207. Ranzani-Paiva, M. J. T., A. T. Silva-Souza, G. C. Pavanelli & R. Wilson, C. B. 2000. North American parasite of the family M. Takemoto. 2000. Hematological characteristics and relative Argulidae, with bibliography of the group and a systematic condition factor (Kn) associated with parasitism in Schizodon review of all know species. United State National Museum, 25: borelli (Osteichthyes, Anostomidae) and Prochilodus lineatus 625-742. (Ostheichtyes, Prochilodontidae) from Parana River, Porto Wolfe, B. A., C. A. Harms, J. D. Groves & M. R. Loomis. 2001. Rico region, Parana, Brazil. Acta Scientiarum Biological Treatment of Argulus sp. infestation of river frogs. Contemporary Sciences, 22: 515-521. Topics in Laboratory Animal Science, 40: 35-36. Ringuelet, R. 1943. Revision de los Argúlidos Argentinos (Crustácea: Yamaguti, S. 1963. Parasitic Copepoda and Branchiura of fishes. Branchiura) com el catallogo de las espesies neotropicales. Revista New York, Interscience Publishers, 1104p. del Museo de La Plata (Seccion Zoologia), 3: 43-99. Zar, J. H. 1996. Biostatistical Analysis. New Jersey, Prentice-Hall, 662p.

Submitted March 6, 2012 Accepted August 8, 2012 Published September 28, 2012